You are on page 1of 7

Original Paper

Eur Neurol 2015;73:164–170 Received: September 30, 2014


Accepted: November 30, 2014
DOI: 10.1159/000370240
Published online: January 13, 2015

Timing of Neurological Improvement


after Acute Ischemic Stroke and
Functional Outcome
Young-Mok Song Geun Ho Lee Jae Il Kim 
Department of Neurology, Dankook University Hospital, Cheonan, South Korea

Key Words Introduction


Stroke · Neurological improvement · Outcome
The clinical course and prognosis of stroke patients are
highly variable. Therefore, the prediction of outcome after
Abstract acute stroke has been an important research issue. The
Background: The time of neurological improvement (TNI) stroke outcome is influenced by multiple factors. Some fac-
after acute ischemic stroke may have a predictive value. tors, such as age and the initial National Institutes of Health
Methods: We evaluated 410 consecutive patients who were Stroke Scale (NIHSS) score [1], have been recognized as
admitted within 12 hours of stroke onset. The National Insti- prognostic factors [2–7]. However, the current predictors
tutes of Health Stroke Scale (NIHSS) was measured on ad- are not sufficient for precise prediction of prognosis, and
mission and at 1, 3, 7, and 14 days. Neurological improve- identification of more predictive factors is necessary.
ment was defined as an improvement in the NIHSS score by The clinical course during the acute phase of stroke may
≥2 points (NI2) or ≥4 points (NI4) or an NIHSS score of 0. have a predictive value. Indeed, it has been reported that
Patients with a Modified Rankin scale (mRS) score of ≤2 were patients who improved within the first 48 hours of stroke
considered to have a good outcome. Results: Patients with onset had a better prognosis [8, 9], suggesting that early
earlier TNIs had a lower 3-month mRS score and a higher neurological improvement is predictive of a good progno-
probability for a good outcome. In the binary and ordinal sis. However, a detailed relationship between the time of
regression analyses, age, NIHSS score, atrial fibrillation and neurological improvement (TNI) and functional outcome
TNI were independently associated with a good outcome. has not been elucidated. The purpose of this study was to
Receiver operating characteristic curve analyses demon- investigate the relationship between the TNI after acute
strated that TNI2 had higher sensitivity and lower specificity ischemic stroke and functional outcome at 3 months.
than TNI4. The best threshold for predicting outcome was
day 3 for TNI2 and day 14 for TNI4. Conclusions: These re-
sults suggest that TNI is independently associated with Methods
functional outcome at 90 days. TNI2 may be more useful We prospectively studied consecutive patients with acute isch-
than TNI4 for early prediction of stroke outcome. emic stroke who were admitted to the Dankook University hospi-
© 2015 S. Karger AG, Basel tal between January 2010 and December 2013. A total of 579 pa-
130.241.16.16 - 11/15/2017 8:33:38 PM

© 2015 S. Karger AG, Basel Young-Mok Song, MD


0014–3022/15/0734–0164$39.50/0 Department of Neurology, Dankook University Hospital
119, Dandae-ro, Dongnam-gu
Göteborgs Universitet

E-Mail karger@karger.com
Cheonan, Chungnam, 330–714 (South Korea)
www.karger.com/ene
Downloaded by:

E-Mail ymsong @ medimail.co.kr
tients eligible for the study had focal neurologic deficits with rel- covariates related to dichotomized mRS in the binary logistic re-
evant lesions on diffusion-weighted imaging and were examined gression analysis. Receiver operating characteristic (ROC) curve
within 12 h of symptom onset. Among them, we excluded the pa- analysis was conducted to evaluate the usefulness of the TNI2 and
tients who had preexisting neurological deficits (65 patients), those TNI4 for predicting a good outcome. We assessed the discrimina-
who received thrombolytic therapy (57 patients), and those who tion by calculating the area under the ROC curve of sensitivity
did not undergo complete workups (22 patients) or were lost to versus 1 minus the specificity. The sensitivity, specificity, and pos-
follow-up (25 patients). Thus, 410 patients with acute ischemic itive and negative predictive values of the TNI2 and TNI4 were
stroke were finally selected for the analyses. calculated to validate the TNIs in predicting a good outcome at
Demographic data and stroke risk factors were recorded in 3 months.
the registry. Data on risk factors were collected and defined as Statistical significance was established at p < 0.05. Statistical
follows: hypertension was defined as repeated detection of blood analyses were performed using SPSS (version 18.0, Chicago, Ill.,
pressure >140/90 mm Hg before stroke or use of antihypertensive USA) and Medcalc (version 13.3).
medication; diabetes mellitus was defined as repeated detection
of fasting blood glucose level >140 mg/dl before stroke or use of
antidiabetic medication; hypercholesterolemia was defined as re-
peated detection of total cholesterol >220 mg/dl or use of lipid- Results
lowering medication; smoking was defined as current smoking
at the time of stroke; and potential sources of cardioembolism There were 243 men and 167 women, and the mean age
were defined as atrial fibrillation, myocardial infarction within was 65.6 ± 11.9 years (range, 26–93 years). The TNI2 was
6 weeks, congestive heart failure, mitral stenosis, and prosthetic day 1 in 95 (23%) patients, day 3 in 131 (32%) patients,
valve.
All of the patients underwent laboratory workups that included day 7 in 92 (22%) patients, day 14 in 36 (9%) patients, and
brain MRI, MR angiography, transthoracic echocardiography, 12- no improvement within 14 days was observed in 56 (14%)
lead ECG, and standard blood tests. Conventional angiography, patients. The TNI4 was day 1 in 28 (7%) patients, day 3 in
transcranial Doppler, transesophageal echocardiography, and 54 (13%) patients, day 7 in 83 (20%) patients, day 14 in 84
Holter monitoring were performed in selected patients as re- (21%) patients, and no improvement in 161 (39%) pa-
quired. An etiologic subtype of ischemic stroke was classified into
large artery disease, cardioembolism, small vessel disease, and un- tients. The clinical characteristics of patients who showed
determined cause according to the Trial of Org 10172 in Acute different TNI2 and TNI4 are listed in tables 1 and 2. The
Stroke Treatment (TOAST) criteria [10]. mean time from symptom onset to study entry was 4.6 ±
The severity of the neurological deficits was assessed using the 3.3 h. The mean initial NIHSS score was 6.9 ± 5.1 (range,
NIHSS. The NIHSS score was serially measured on admission and 1–29; median, 5; interquartile range, 4–9). There was no
at 1, 3, 7, and 14 days after stroke onset. Neurological improvement
(NI4) was defined as a decrease in the NIHSS score by ≥4 points difference in terms of age, sex, vascular risk factors, and
from the baseline NIHSS score or a NIHSS score of 0. We also con- stroke subtype between patients with different TNI2 or
sidered minor neurological improvement (NI2) as a NIHSS score TNI4. The initial neurological deficits measured by the
change by ≥2 points or a NIHSS score of 0. The time of neurolog- NIHSS were the most severe in patients who showed no
ical improvement (TNI4) or the time of minor neurological im- improvement within 14 days of stroke onset (10.7 ± 7.8
provement (TNI2) was classified into day 1, 3, 7, 14, and no im-
provement. Modified Rankin Scale (mRS) was used to assess the for TNI2, p < 0.01 and 7.6 ± 5.9 for TNI4, p < 0.01).
functional outcome at 3 months [11]. For the purpose of the anal- Patients who showed earlier improvement had a high-
ysis, patients who had an mRS score of 0–2 were considered to have er probability for a good outcome. Most (86% for TNI2
a good outcome. If patients were discharged from the hospital dur- and 92% for TNI4) of the patients who improved within
ing the study period, they were evaluated at the outpatient clinic one day had a good outcome and the rate of good out-
on the scheduled day. If patients could not visit the hospital at
3  months because of severe disability or other causes, the mRS come decreased as the neurological improvement oc-
score was measured by a telephone interview. curred later. Of the patients who did not show improve-
ment within 14 days, 30% (TNI2) and 52% (TNI4) of
Statistical Analysis them achieved a good outcome.
A comparison of the baseline characteristics and outcome pro- Univariate logistic regression analysis revealed that
files among patients with different time of neurological improve-
ment was performed by the ANOVA test for continuous variables the outcome was associated with age, NIHSS score, atrial
and by the χ2 test for dichotomized variables. Binary logistic and fibrillation, stroke subtype, TNI2, and TNI4 (table  3).
ordinal regression analyses were used to assess the effects of TNIs Among these variables, age, NIHSS score, atrial fibrilla-
on clinical outcome adjusted for variables showing a p < 0.2 in tion, and TNI2 or TNI4 were selected in the final model
univariate analysis. In binary logistic models, mRS was dichoto- (table 4). TNI2 (OR, 2.23; 95% CI, 1.73–2.87; p < 0.01)
mized (mRS ≤2 vs. mRS >2) and a backward stepwise strategy was
used to select the variables remaining in the final model. We con- and TNI4 (OR, 2.30; 95% CI, 1.71–3.10; p < 0.01) were
structed ordinal regression models to verify that the results were independently associated with an outcome at 90 days in
consistent across the levels of the mRS adjusted for factors and the adjusted binary regression model. Ordinal regression
130.241.16.16 - 11/15/2017 8:33:38 PM

Timing of Improvement and Stroke Eur Neurol 2015;73:164–170 165


Outcome DOI: 10.1159/000370240
Göteborgs Universitet
Downloaded by:
Table 1. Clinical characteristics of patients with different time of minor neurological improvement (TNI2)

Day 1 Day 3 Day 7 Day 14 No NI p

Patients, n 95 131 92 36 56
Age, years (mean ± SD) 66.1±12.4 64.5±11.4 64.6±11.5 63.8±12.8 69.9±12.0 0.39
Males, n (%) 61 (64) 75 (57) 58 (63) 21 (58) 28 (50) 0.44
Time from onset to entry, h (mean ± SD) 3.9±3.2 5.3±3.6 6.0±3.8 3.9±2.2 3.5±2.2 <0.01
Initial NIHSS score (mean ± SD) 6.5±4.2 6.3±4.2 6.0±3.6 6.4±4.6 10.7±7.8 <0.01
Median (interquartile range) 5 (3–9) 5 (3.25–8) 5 (4–7.5) 5 (3.75–7.25) 9.5 (4.25–17.75)
Risk factors, n (%)
Hypertension 61 (64) 80 (61) 61 (66) 21 (58) 39 (70) 0.74
Diabetes mellitus 19 (20) 37 (28) 26 (28) 10 (28) 19 (34) 0.42
Hyperlipidemia 24 (25) 23 (18) 25 (27) 11 (31) 8 (14) 0.14
Smoking 24 (25) 43 (33) 34 (37) 13 (36) 18 (32) 0.51
Atrial fibrillation 26 (27) 18 (14) 17 (19) 7 (19) 17 (30) 0.04
Previous stroke 18 (19) 22 (17) 10 (11) 9 (25) 9 (16) 0.35
Stroke subtypes, n (%) 0.06
Large artery disease 27 (28) 41 (31) 24 (26) 10 (28) 17 (30)
Cardioembolism 23 (24) 19 (15) 15 (16) 6 (17) 20 (36)
Small vessel disease 31 (33) 50 (38) 39 (42) 16 (44) 9 (16)
Undetermined 14 (15) 21 (16) 14 (15) 4 (11) 10 (18)
mRS at 3 months (mean ± SD) 1.3±1.1 1.6±1.3 1.8±1.3 2.3±1.4 3.8±1.8 <0.01
Good outcome*, n (%) 82 (86) 102 (78) 67 (73) 21 (59) 17 (30) <0.01

* Modified Rankin Scale score at 3 months after stroke ≤2.

Table 2. Clinical characteristics of patients with different time of neurological improvement (TNI4)

Day 1 Day 3 Day 7 Day 14 No NI p

Patients, n 28 54 83 84 161
Age, years (mean ± SD) 63.1±14.7 65.5±10.3 66.0±11.7 65.5±11.0 65.8±12.6 0.85
Males, n (%) 21 (75) 31 (57) 49 (59) 47 (56) 95 (59) 0.50
Time from onset to entry, h (mean ± SD) 2.7±2.9 3.8±3.5 4.7±3.0 5.9±3.3 4.5±3.4 0.02
Initial NIHSS score (mean ± SD) 6.7±4.4 6.6±4.3 6.0±4.5 6.5±4.3 7.6±5.9 0.15
Median (interquartile range) 6 (2.75–9.25) 5 (4–10) 5 (3–8) 5 (4–8) 6 (4–10)
Risk factors, n (%)
Hypertension 16 (57) 37 (69) 51 (61) 52 (62) 109 (68) 0.67
Diabetes mellitus 5 (18) 11 (20) 27 (33) 25 (30) 43 (27) 0.41
Hyperlipidemia 5 (18) 16 (30) 23 (28) 20 (24) 27 (17) 0.17
Smoking 9 (32) 19 (35) 35 (42) 30 (36) 51 (32) 0.60
Atrial fibrillation 10 (36) 9 (17) 16 (19) 13 (16) 37 (23) 0.17
Previous stroke 4 (14) 7 (13) 17 (21) 13 (16) 27 (17) 0.81
Stroke subtypes, n (%) 0.43
Large artery disease 7 (25) 15 (28) 27 (33) 27 (32) 43 (27)
Cardioembolism 10 (36) 9 (17) 14 (17) 12 (14) 38 (24)
Small vessel disease 8 (29) 19 (35) 26 (31) 31 (37) 61 (38)
Undetermined 3 (11) 11 (20) 16 (19) 14 (17) 19 (12)
mRS at 3 months (mean ± SD) 0.7±1.1 1.4±1.2 1.6±1.3 1.7±1.5 2.8±1.8 <0.01
Good outcome*, n (%) 26 (92) 44 (82) 63 (76) 65 (74) 84 (52) <0.01

* Modified Rankin Scale score at 3 months after stroke ≤2.


130.241.16.16 - 11/15/2017 8:33:38 PM

166 Eur Neurol 2015;73:164–170 Song/Lee/Kim


DOI: 10.1159/000370240
Göteborgs Universitet
Downloaded by:
Table 3. Univariate binary logistic regression analysis for a good 65%; positive predictive value, 81%; negative predictive
outcome value, 43%) and day 14 for TNI4 (sensitivity, 68%; speci-
ficity, 61%; positive predictive value, 79%; negative pre-
Good outcome (mRS ≤2)
dictive value, 48%).
p OR (95% CI)

Age <0.01 0.96 (0.94–0.98)


Sex, male 0.10 1.43 (0.93–2.19) Discussion
Time from onset to entry 0.12 1.09 (0.98–1.21)
Initial NIHSS score <0.01 0.72 (0.67–0.78) The effect of early neurological improvement on out-
Risk factors come has been mostly studied in clinical trials with
Hypertension 0.47 1.18 (0.76–1.82)
Diabetes mellitus 0.28 0.78 (0.49–1.24) thrombolytic treatment [12–15]. They focused on the im-
Hypercholesterolemia 0.69 1.11 (0.66–1.85) mediate clinical response with recanalization after throm-
Smoking 0.50 1.18 (0.74–1.85) bolysis. Although a majority of stroke patients do not re-
Atrial fibrillation <0.01 0.35 (0.21–0.57) ceive thrombolytic therapy, only a few studies analyzed
Previous stroke 0.68 0.89 (0.51–1.55) the effect of early spontaneous improvement on outcome.
Stroke subtypes
Large artery disease 0.08 0.55 (0.29–1.07) Our data suggest that earlier improvement is associated
Cardioembolism 0.04 0.47 (0.24–0.95) with a better 3-month mRS score and a higher likelihood
Small vessel disease <0.01 2.82 (1.35–5.90) of functional independence in patients who are not treat-
Undetermined 1 ed with thrombolytic agents. A previous study by Toni
TNI2 et  al. analyzed the TNI limited to 48 h [9]. They ob-
Day 1 <0.01 14.23 (6.0–33.88)
Day 3 <0.01 8.41 (4.29–16.50) served that improving patients (an improvement of the
Day 7 <0.01 6.35 (3.10–13.01) Canadian Neurological Scale score ≥1 point) within the
Day 14 0.07 3.33 (1.39–8.02) first 48 h after stroke had a lower fatality and disability,
No improvement 1 and improvement within 48 h was independently associ-
TNI4
ated with a good outcome. The present study provided
Day 1 0.01 11.07 (2.52–48.52)
Day 3 <0.01 4.20 (1.91–9.26) more detailed information on the relationship between
Day 7 0.01 2.88 (1.51–5.51) the TNIs up to 14 days and the stroke outcome. More-
Day 14 0.03 2.26 (1.37–4.80) over, the association between the TNI and outcome was
No improvement 1 further verified in ordinal regression analysis, which
OR = Odds ratio; CI = confidence interval.
might complement the limitation of dichotomized out-
come analysis. The concept that patients with earlier im-
provement had a better prognosis may be generally ap-
plied to the acute period of stroke.
We compared the predictive value of TNI2 and TNI4
analysis demonstrated a significant shift toward a better in the ROC analysis. Both TNIs showed a similar area un-
mRS scale in patients with earlier TNI2 (OR, 1.97; 95% der the ROC curve (0.701 vs. 0.671, p = 0.54), but TNI2
CI, 1.70–2.31; p < 0.01) or earlier TNI4 (OR, 2.10; 95% CI, showed a higher sensitivity and lower specificity than
1.79–2.47; p < 0.01). When the TNIs were categorized TNI4. The best cut-off time for predicting outcome was
into each period, the TNIs of earlier periods showed a day 3 for TNI2 (sensitivity, 63%; specificity, 65%) and day
higher odds ratio for a good outcome in binary and ordi- 14 for TNI4 (sensitivity, 65%; specificity, 61%). Thus,
nal analyses (table 4). TNI2 is better than TNI4 for early prediction of outcome.
The ROC curve for TNI2 and TNI4 that predict a good In addition, using TNI2 yielded a higher number of sub-
outcome is shown in figure 1. The area under the ROC jects for analysis. About 39% of patients were classified as
curve did not differ significantly between TNI2 and TNI4 those with no improvement using the TNI4 criteria,
(0.701 vs. 0.671, p = 0.54). Overall, using TNI2 for predic- whereas only 14% of patients were classified as those with
tion of 90-day outcome showed higher sensitivity and no improvement according to the TNI2 criteria.
lower specificity than using TNI4, but the positive and Most studies on thrombolytic treatment have adopted
negative predictive values were similar between TNI2 and the definition of neurological improvement requiring a
TNI4 (table 5). The best threshold for predicting a good change of ≥4 points or ≥8 points in the NIHSS score [12–
outcome was day 3 for TNI2 (sensitivity, 63%; specificity, 14]. Patients with a low baseline NIHSS score may be less
130.241.16.16 - 11/15/2017 8:33:38 PM

Timing of Improvement and Stroke Eur Neurol 2015;73:164–170 167


Outcome DOI: 10.1159/000370240
Göteborgs Universitet
Downloaded by:
Table 4. Multivariate binary logistic and ordinal regression models for outcome including the TNI2 or TNI4

Binary logistic analysis Ordinal analysis


(mRS ≤2 vs. mRS >2) (mRS 0–6)
p OR (95% CI) p OR (95% CI)

Age 0.04 0.97 (0.95–0.99) 0.01 0.97 (0.96–0.99)


Atrial fibrillation 0.01 0.27 (0.13–0.58) <0.01 0.36 (0.23–0.58)
Initial NIHSS <0.01 0.69 (0.63–0.75) <0.01 0.75 (0.72–0.79)
TNI2
Day 1 <0.01 31.08 (9.21–104.9) <0.01 22.02 (10.78–44.96)
Day 3 <0.01 8.66 (3.44–21.84) <0.01 8.58 (4.63–15.87)
Day 7 0.01 5.00 (1.93–12.81) <0.01 6.65 (3.46–12.78)
Day 14 0.26 1.88 (0.62–5.72) 0.02 3.45 (1.55–7.67)
No improvement 1 1
Age 0.06 0.98 (0.95–1.00) 0.02 0.97 (0.96–0.99)
Atrial fibrillation <0.01 0.30 (0.13–0.67) <0.01 0.32 (0.19–0.55)
Initial NIHSS <0.01 0.69 (0.63–0.75) <0.01 0.74 (0.70–0.77)
TNI4
Day 1 <0.01 28.98 (4.90–171.3) <0.01 37.96 (15.14–95.15)
Day 3 <0.01 12.12 (3.91–37.59) <0.01 7.12 (3.83–13.24)
Day 7 <0.01 4.95 (2.03–12.12) <0.01 4.31 (2.49–7.46)
Day 14 0.03 3.47 (1.54–7.84) <0.01 3.98 (2.32–6.84)
No improvement 1 1

OR = Odds ratio; CI = confidence interval.

likely to meet these criteria of neurological improvement


ROC curve
unless they reach a NIHSS score of 0. We addressed this
1.0 concern by analyzing the minor neurological improve-
ment with a change of ≥2 points on the NIHSS score
(TNI2). In contrast to clinical trials with thrombolytic
0.8 treatment in which moderate severity of stroke patients
were mainly enrolled, this study included all severity of
stroke patients covering patients with a minor stroke. In-
0.6 deed, the baseline NIHSS score (median, 5) of this study
Sensitivity

population was lower than that of clinical trials (median,


9, 14 or 17) [15–18]. Therefore, the criteria of TNI2 may
0.4 be more sensitive than that of TNI4 for prediction of out-
come in this population.
In previous reports, several clinical characteristics
0.2
including NIHSS score, age, and atrial fibrillation have
shown to influence the functional outcome [2–7, 19]. In
TNI2 our regression analysis, these variables were also identi-
TNI4
fied as independent predictors, corroborating the re-
0
0 0.2 0.4 0.6 0.8 1.0 sults of previous studies. With regard to stroke subtype,
1 – specificity lacunar stroke or dysarhria-clumsy hand syndrome has
been suggested as a significant predictor of spontaneous
good outcome [5, 20]. In our study, lacunar infarction
Fig. 1. ROC curve comparing TNI2 and TNI4 for predicting a good was associated with a good outcome, but after multi-
outcome. variate adjustment, the association was not significant.
130.241.16.16 - 11/15/2017 8:33:38 PM

168 Eur Neurol 2015;73:164–170 Song/Lee/Kim


DOI: 10.1159/000370240
Göteborgs Universitet
Downloaded by:
Table 5. The sensitivity, specificity, and positive and negative predictive values with 95% confidence intervals of TNI2 and TNI4 for
predicting a good outcome (mRS ≤2)

Sensitivity Specificity + Predictive value – Predictive value


Criteria TNI2 TNI4 TNI2 TNI4 TNI2 TNI4 TNI2 TNI4

Day 1 21.3 (16.7–26.5) 9.92 (6.5–14.4) 91.9 (85.7–96.1) 98.3 (93.9–99.8) 85.9 (75.6–93.0) 92.3 (74.9–99.1) 33.6 (28.6–38.9) 34.3 (29.2–39.7)
Day 3 62.9 (57.1–68.5) 26.9 (21.4–32.9) 65.3 (56.3–73.6) 90.5 (83.7–95.2) 80.7 (74.9–85.7) 85.5 (75.6–92.5) 43.3 (36.1–50.7) 37.2 (31.6–43.2)
Day 7 86.7 (82.2–90.4) 47.5 (41.1–54.0) 45.2 (36.2–54.3) 76.7 (68.0–84.1) 78.5 (73.5–82.9) 81.0 (73.6–87.1) 59.6 (49.0–69.6) 41.2 (34.6–48.1)
Day 14 93.7 (90.2–96.2) 68.2 (61.9–74.0) 33.9 (25.6–42.9) 61.2 (51.7–70.1) 76.6 (71.8–80.9) 78.6 (72.4–83.9) 70.0 (56.8–81.2) 48.0 (39.7–56.3)

The association may depend on the NIHSS score or oth- cated as the baseline characteristics of thrombolysis-
er factors. treated patients were specific and distinct from those of
This study has some limitations. As we recruited acute patients who were not treated with thrombolysis. The
ischemic stroke patients within 12 h after onset, the pa- clinical implication may also differ between spontaneous
tients who had already improved prior to hospital arrival improvement and improvement associated with throm-
may have not been considered having neurological im- bolytic treatment. Further studies, however, including
provement. The frequency of patients with a certain pe- thrombolysis-treated patients and adjusting these factors
riod of TNI, especially a TNI of day 1, may vary depend- will provide more valuable information.
ing on the time elapsed from stroke onset to admission. In conclusion, our data suggest that TNI after acute
Nevertheless, the data are clinically valuable because ischemic stroke is independently associated with func-
some delay from stroke onset to hospital arrival is also tional outcome at 90 days. In addition to initial NIHSS
present in clinical setting. score and age, the TNI can be a valid predictor of the
We did not exclude patients who improved to no def- stroke outcome. TNI2 may be more useful than TNI4 for
icit at day 1 (transient ischemic attack, TIA) if they had early prediction of outcome in patients who did not re-
neurological deficits on admission and had a relevant le- ceive thrombolytic therapy.
sion on DWI. According to the tissue-based definition of
TIA, only traditional TIA without evidence of acute in-
farction on brain imaging is classified as TIA [21]. Thus, Disclosure Statement
we classified these patients as stroke patients. Although
None.
this classification is controversial, such patients were
small in number (8 patients) and may have not affected
the overall results.
Funding
We excluded patients treated with thrombolysis, be-
cause our study focused on the natural course of stroke, The present research was conducted by the research fund of
and statistical analyses and interpretation were compli- Dankook University in 2013.

References
1 Brott T, Adams HP Jr, Olinger CP, Marler JR, 4 Henon H, Godefroy O, Leys D, Mounier-Ve- 6 Weimar C, Konig IR, Kraywinkel K, Ziegler
Barsan WG, Biller J, Spilker J, Holleran R, Eb- hier F, Lucas C, Rondepierre P, Duhamel A, A, Diener HC; German Stroke Study Collabo-
erle R, Hertzberg V: Measurements of acute Pruvo JP: Early predictors of death and dis- ration: Age and National Institutes of Health
cerebral infarction: a clinical examination ability after acute cerebral ischemic event. Stroke Scale Score within 6 hours after onset
scale. Stroke 1989;20:864–870. Stroke 1995;26:392–398. are accurate predictors of outcome after cere-
2 Kotila M, Waltimo O, Niemi ML, Laaksonen 5 Adams HP Jr, Davis PH, Leira EC, Chang KC, bral ischemia: development and external vali-
R, Lempinen M: The profile of recovery from Bendixen BH, Clarke WR, Woolson RF, Han- dation of prognostic models. Stroke 2004; 35:
stroke and factors influencing outcome. sen MD: Baseline NIH Stroke Scale score 158–162.
Stroke 1984;15:1039–1044. strongly predicts outcome after stroke: a re- 7 Muir KW, Weir CJ, Murray GD, Povey C,
3 Wade DT, Wood VA, Hewer RL: Recovery af- port of the Trial of Org 10172 in Acute Stroke Lees KR: Comparison of neurological scales
ter stroke – the first 3 months. J Neurol Neu- Treatment (TOAST). Neurology 1999; 53: and scoring systems for acute stroke progno-
rosurg Psychiatry 1985;48:7–13. 126–131. sis. Stroke 1996;27:1817–1820.
130.241.16.16 - 11/15/2017 8:33:38 PM

Timing of Improvement and Stroke Eur Neurol 2015;73:164–170 169


Outcome DOI: 10.1159/000370240
Göteborgs Universitet
Downloaded by:
8 Wityk RJ, Pessin MS, Kaplan RF, Caplan LR: 14 Hemmen TM, Ernstrom K, Raman R: Two- 18 Furlan A, Higashida R, Wechsler L, Gent M,
Serial assessment of acute stroke using the hour improvement of patients in the National Rowley H, Kase C, Pessin M, Ahuja A, Calla-
NIH Stroke Scale. Stroke 1994;25:362–365. Institute of Neurological Disorders and han F, Clark WM, Silver F, Rivera F: Intra-
9 Toni D, Fiorelli M, Bastianello S, Falcou A, Stroke trials and prediction of final outcome. arterial prourokinase for acute ischemic
Sette G, Ceschin V, Sacchetti ML, Argentino Stroke 2011;42:3163–3167. stroke. The PROACT II study: a randomized
C: Acute ischemic strokes improving during 15 Kharitonova T, Mikulik R, Roine RO, Soinne controlled trial. Prolyse in Acute Cerebral
the first 48 hours of onset: predictability, out- L, Ahmed N, Wahlgren N; Safe Implementa- Thromboembolism. JAMA 1999; 282: 2003–
come, and possible mechanisms. A compari- tion of Thrombolysis in Stroke Investigators: 2011.
son with early deteriorating strokes. Stroke Association of early National Institutes of 19 Kimura K, Minematsu K, Yamaguchi T;
1997;28:10–14. Health Stroke Scale improvement with vessel Japan Multicenter Stroke Investigators’ Col-
10 Adams HP Jr, Bendixen BH, Kappelle LJ, Bill- recanalization and functional outcome after laboration (J-MUSIC): Atrial fibrillation as a
er J, Love BB, Gordon DL, Marsh EE 3rd: Clas- intravenous thrombolysis in ischemic stroke. predictive factor for severe stroke and early
sification of subtype of acute ischemic stroke. Stroke 2011;42:1638–1643. death in 15,831 patients with acute ischaemic
Definitions for use in a multicenter clinical 16 Hacke W, Kaste M, Bluhmki E, Brozman M, stroke. J Neurol Neurosurg Psychiatry 2005;
trial. TOAST. Trial of Org 10172 in Acute Dávalos A, Guidetti D, Larrue V, Lees KR, 76:679–683.
Stroke Treatment. Stroke 1993;24:35–41. Medeghri Z, Machnig T, Schneider D, von 20 Arboix A, García-Eroles L, Comes E, Oliveres
11 Wolfe CD, Taub NA, Woodrow EJ, Burney Kummer R, Wahlgren N, Toni D; ECASS In- M, Balcells M, Pacheco G, Targa C: Predicting
PG: Assessment of scales of disability and vestigators: Thrombolysis with alteplase 3 to spontaneous early neurological recovery after
handicap for stroke patients. Stroke 1991; 22: 4.5 hours after acute ischemic stroke. N Engl acute ischemic stroke. Eur J Neurol 2003; 10:
1242–1244. J Med 2008;359:1317–1329. 429–435.
12 Brown DL, Johnston KC, Wagner DP, Haley 17 Tissue plasminogen activator for acute isch- 21 Easton JD, Saver JL, Albers GW, Alberts MJ,
EC Jr: Predicting major neurological im- emic stroke. The National Institute of Neuro- Chaturvedi S, Feldmann E, Hatsukami TS,
provement with intravenous recombinant tis- logical Disorders and Stroke rt-PA Stroke Higashida RT, Johnston SC, Kidwell CS, Lut-
sue plasminogen activator treatment of Study Group. N Engl J Med 1995; 333: 1581– sep HL, Miller E, Sacco RL: Definition and
stroke. Stroke 2004;35:147–150. 1587. evaluation of transient ischemic attack: a
13 Saposnik G, Di Legge S, Webster F, Hachinski scientific statement for healthcare profession-
V: Predictors of major neurologic improve- als from the American Heart Association/
ment after thrombolysis in acute stroke. Neu- American Stroke Association. Stroke 2009;40:
rology 2005;65:1169–1174. 2276–2293.

130.241.16.16 - 11/15/2017 8:33:38 PM

170 Eur Neurol 2015;73:164–170 Song/Lee/Kim


DOI: 10.1159/000370240
Göteborgs Universitet
Downloaded by:

You might also like